Abstract
Polyomaviruses are small, tumorigenic, nonenveloped viruses that infect several different species. Interaction of these viruses with cell surface receptors represents the initial step during infection of host cells. This interaction can be a major determinant of viral host and tissue tropism. This chapter reviews what is currently known about the cellular receptors for each of five polyomavirus family members: Mouse polyomavirus (PyV), JC virus (JCV), BK virus (BKV), Lymphotropic papovavirus (LPV) and Simian virus 40 (SV40). These polyomaviruses serve to illustrate the enormous diversity of virus-cell surface interactions and allow us to closely evaluate the role of receptors in their life cycles. The contribution of other factors such as transcriptional regulators and signaling pathways are also summarized.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Preview
Unable to display preview. Download preview PDF.
References
Eckhart W. Polyomavirinae and their replication. In: Fields BN, Knipe DM, eds. Virology Raven Press, 1994.
Keller W, Muller U, Eicken I et al. Biochemical and ultrastructural analysis of SV40 chromatin. Cold Spring Harb Symp Quant Biol 1978; 42 (Pt 1):227–44.
Imperiale MJ. The human polyomaviruses, BKV and JCV: Molecular pathogensis of acute disease and potential role in cancer. Virology 2000; 267:1–7.
Frisque RJ, Bream GL, Cannella MT. Human polyomavirus JC virus genome. J Virol 1984; 51(2):458–69.
Pho MT, Ashok A, Atwood WJ. JC Virus enters human glial cells by clathrin dependent receptor mediated endocytosis. J Virol 2000; 74(5):2288–92.
Gilbert JM, Benjamin TL. Early steps of polyomavirus entry into cells. J Virol 2000; 74(18):8582–8.
Richterova Z, Liebl D, Horak M et al. Caveolae are involved in the trafficking of mouse polyomavirus virions and artificial VP1 pseudocapsids toward cell nuclei. J Virol 2001; 75(22):10880–91.
Anderson HA, Chen Y, Norkin LC. Bound simian virus 40 translocates to caveolin enriched membrane domains, and its entry is inhibited by drugs that selectively disrupt caveolae. Molecular Biology of the Cell 1996; 7:1825–34.
Ashok A, Atwood WJ. Contrasting roles of endosomal pH and the cytoskeleton in infection of human glial cells by JC virus and simian virus 40. J Virol 2003; 77(2):1347–56.
Pelkmans L, Kartenbeck J, Helenius A. Caveolar endocytosis of simian virus 40 reveals a new two-step vesicular-transport pathway to the ER. Nat Cell Biol 2001; 3(5):473–83.
Gilbert JM, Goldberg IG, Benjamin TL. Cell penetration and trafficking of polyomavirus. J Virol 2003; 77(4):2615–22.
Kasamatsu H, Lin W, Edens J et al. Visualization of antigens attached to cytoskeletal framework in animal cells: Colocalization of simian virus 40 Vp1 polypeptide and actin in TC7 cells. Proc Natl Acad Sci USA 1983; 80(14):4339–43.
Nakanishi A, Clever J, Yamada M et al. Association with capsid proteins promotes nuclear targeting of simian virus 40 DNA. Proc Natl Acad Sci USA 1996; 93(1):96–100.
Yamada M, Kasamatsu H. Role of nuclear pore complex in simian virus 40 nuclear targeting. J Virol 1993; 67(1):119–30.
Nakanishi A, Shum D, Morioka H et al. Interaction of the Vp3 nuclear localization signal with the importin alpha 2/beta heterodimer directs nuclear entry of infecting simian virus 40. J Virol 2002; 76(18):9368–77.
Dawe CJ, Freund R, Mandel G et al. Variations in polyoma virus genotype in relation to tumor induction in mice. Characterization of wild type strains with widely differing tumor profiles. Am J Pathol 1987; 127(2):243–61.
Fried H, Cahan LD, Paulson JC. Polyoma virus recognizes specific sialyligosaccharide receptors on host cells. Virology 1981; 109(1):188–92.
Cahan LD, Singh R, Paulson JC. Sialyloligosaccharide receptors of binding variants of polyomavirus. Virology 1983; 130:281–89.
Fried H, Cahan LD, Paulson JC. Polyomavirus recognizes specific sialyligosaccharide receptors. Virology 1981; 109:188–92.
Diamond L, Crawford LV. Some characteristics of large plaque and small plaque lines of polyomavirus. Virology 1964; 22:235–44.
Freund R, Calderone A, Dawe CJ et al. Polyomavirus tumor induction in mice, effects of polymorphisms of VP1 and large T antigen. J Virol 1991; 65:335–41.
Stehle T, Yan Y, Benjamin TL et al. Structure of murine polyomavirus complexed with an oligosaccharide receptor fragment. Nature 1994; 369(6476):160–3.
Stehle T, Harrison SC. High-resolution structure of a polyomavirus VP1-oligosaccharide complex: Implications for assembly and receptor binding. EMBO J 1997; 16(16):5139–48.
Bauer PH, Cui C, Stehle T et al. Discrimination between sialic acid containing receptors and pseudoreceptors regulates polyomavirus spread in the mouse. J Virol 1999; 73:5826–32.
Chen MH, Benjamin T. Roles of N-glycans with alpha 2,6 as well as alpha 2,3 linked sialic acid in infection by polyoma virus. Virology 1997; 233:440–42.
Griffith GR, Consigli RA. Cross-Linking of a polyoma attachment protein to its mouse kidney cell receptor. J Virol 1986; 58:773–81.
Marriott SJ, Griffith GR, Consigli RA. Octyl-B-D-glucopyranoside extracts polyomavirus receptor moieties from the surfaces of mouse kidney cells. J Virol 1987; 61:375–82.
Marriott SJ, Roeder DJ, Consigli RA. Anti-idiotypic antibodies to a polyomavirus monoclonal antibody recognize. J Virol 1987; 61:2747–53.
Herrmann M, von der Lieth CW, Stehling P et al. Consequences of a subtle sialic acid modification on the murine polyomavirus receptor. J Virol 1997; 71(8):5922–31.
Caruso M, Iacobini C, Passananti C et al. Protein recognition sites in polyomavirus enhancer: Formation of a novel site for NF-1 factor in an enhancer mutant and characterization of a site in the enhancer D domain. Embo J 1990; 9(3):947–55.
Tsai B, Gilbert JM, Stehle T et al. Gangliosides are receptors for murine polyoma virus and SV40. Embo J 2003; 22(17):4346–55.
Dubensky TW, Freund R, Dawe CJ et al. Polyomavirus replication in mice: Influences of VP1 type and route of innoculation. J Virol 1991; 65:342–49.
Amati P. Polyoma regulatory region: A potential probe for mouse cell differentiation. Cell 1985; 43(3 Pt 2):561–2.
Katinka M, Yaniv M, Vasseur M et al. Expression of polyoma early functions in mouse embryonal carcinoma cells depends on sequence rearrangements in the beginning of the late region. Cell 1980; 20(2):393–9.
De Simone V, La Mantia G, Lania L et al. Polyomavirus mutation that confers a cell-specific cis advantage for viral DNA replication. Mol Cell Biol 1985; 5(8):2142–6.
Maione R, Passananti C, De Simone V et al. Selection of mouse neuroblastoma cell-specific polyoma virus mutants with stage differentiative advantages of replication. Embo J 1985; 4(12):3215–21.
Padgett B, ZuRhein G, Walker D et al. Cultivation of papova-like virus from human brain with progressive multifocal leukoencephalopathy. Lancet 1971; I:1257–60.
Monaco MGC, Atwood WJ, Gravell M et al. JCV infection of hematopoetic progenitor cells, primary B lymphocytes, and tonsillar stromal cells: Implication for viral latency. J Virol 1996; 70:7004–12.
Houff SA, Major EO, Katz DA et al. Involvement of JC virus-infected mononuclear cells from the bone marrow and spleen in the pathogenesis of progressive multifocal leukoencephalopathy. N Engl J Med 1988; 318(5):301–5.
Schweighardt B, Atwood WJ. Glial cells as targets of viral infection in the human central nervous system. In: Nieto-Sampedro M, Castellano Lopez B, eds. Glial Cell Function in Health and Disease. Amsterdam: Elsevier Press, 2001:731–45.
Chen BJ, Atwood WJ. Construction of a novel JCV/SV40 hybrid virus (JCSV) reveals a role for the JCV capsid in viral tropism. Virology 2002; 300(2):282–90.
Padgett BL, Walker DL. Virologic and serologic studies of progressive multifocal leukoencephalopathy. Prog Clin Biol Res 1983; 105:107–17.
Liu CK, Hope AP, Atwood WJ. The human polyomavirus, JCV, does not share receptor specificity with SV40 on human glial cells. J Neurovirol 1998; 4:49–58.
Liu CK, Wei G, Atwood WJ. Infection of glial cells by the human polyomavirus JC is mediated by an N-linked glycoprotein containing terminal alpha 2-6 linked sialic acids. J Virol 1998; 72:4643–49.
Eash S, Tavares R, Stopa EG et al. Differential distribution of the JC virus receptor-type sialic acid in normal human tissues. American Journal of Pathology (In Press).
Komagome R, Sawa H, Suzuki T et al. Oligosaccharides as receptors for JC virus. J Virol 2002; 76(24):12992–3000.
Feigenbaum L, Khalili K, Major E et al. Regulation of the host range of human papovavirus JCV. Proc Natl Acad Sci USA 1987; 84(11):3695–8.
Suzuki S, Sawa H, Komagome R et al. Broad distribution of the JC virus receptor contrasts with a marked cellular restriction of virus replication. Virology 2001; 286(1):100–12.
Gee GV, Manley K, Atwood WJ. Derivation of a JC virus-resistant human glial cell line: Implications for the identification of host cell factors that determine viral tropism. Virology 2003; 314(1):101–9.
Amemiya K, Traub R, Durham L et al. Adjacent nuclear factor-1 and activator protein binding sites in the enhancer of the neurotropic JC virus. A common characteristic of many brain-specific genes. J Biol Chem 1992; 267:14204–11.
Chen N, Khalili K. Transcriptional regulation of human JC polyomavirus promoters by cellular proteins YB-1 and Pur alpha in glial cells. J Virol 1995; 69:5843–48.
Henson JW. Regulation of the glial-specific JC virus early promoter by the transcription factor Sp 1. J Biol Chem 1994; 269:1046–50.
Raj GV, Khalili K. Identification and characterization of a novel GGA/C-binding protein, GBP-i, that is rapidly inducible by cytokines. Mol Cell Biol 1994; 14(12):7770–81.
Kerr D, Chang C, Chen N et al. Transcription of a human neurotropic virus promoter in glial cells: Effect of YB-1 on expression of the JC virus late gene. J Virol 1994; 68:7637–43.
Ranganathan PN, Khalili K. The transcriptional enhancer element, kappa B, regulates promoter activity of the human neurotropic virus, JCV, in cells derived from the CNS. Nucleic Acids Res 1993; 21(8):1959–64.
Wegner M, Drolet DW, Rosenfeld MG. Regulation of JC virus by the POU-domain transcription factor Tst-1: Implications for progressive multifocal leukoencephalopathy. Proc Nat Acad Sci 1993; 90:4743–47.
Monaco MC, Sabath BF, Durham LC et al. JC virus multiplication in human hematopoietic progenitor cells requires the NF-1 class D transcription factor. J Virol 2001; 75(20):9687–95.
Elsner C, Dorries K. Human polyomavirus JC control region variants in persistently infected CNS and kidney tissue. J Gen Virol 1998; 79 (Pt 4):789–99.
Shinohara T, Matsuda M, Yasui K et al. Host range bias of the JC virus mutant enhancer with DNA rearrangement. Virology 1989; 170(1):261–3.
Pfister LA, Letvin NL, Koralnik IJ. JC virus regulatory region tandem repeats in plasma and central nervous system isolates correlate with poor clinical outcome in patients with progressive multifocal leukoencephalopathy. J Virol 2001; 75(12):5672–6.
Wei G, Liu CK, Atwood WJ. JC Virus binds to primary human glial cells, tonsillar stromal cells, and B-lymphocytes, but not to T-lymphocytes. J Neurovirol 2000; 6(2):127–36.
Andreoletti L, Dubois V, Lescieux A et al. Human polyomavirus JC latency and reactivation status in blood of HIV-1-positive immunocompromised patients with and without progressive multifocal leukoencephalopathy. Aids 1999; 13(12):1469–75.
Atwood WJ, Amemiya K, Traub R et al. Interaction of the human polyomavirus, JCV, with human B-lymphocytes. Virology 1992; 190:716–23.
Hashida Y, Gaffney PC, Yunis EJ. Acute hemorrhagic cystitis of childhood and papovavirus-like particles. J Pediatr 1976; 89(1):85–7.
Binet I, Nickeleit V, Hirsch HH et al. Polyomavirus disease under new immunosuppressive drugs: A cause of renal graft dysfunction and graft loss. Transplantation 1999; 67(6):918–22.
Nickeleit V, Singh HK, Mihatsch MJ. Polyomavirus nephropathy: Morphology, pathophysiology, and clinical management. Curr Opin Nephrol Hypertens 2003; 12(6):599–605.
Takemoto KK, Mullarkey MF. Human papovavirus, BK strain: Biological studies including antigenic relationship to simian virus 40. J Virol 1973; 12(3):625–31.
Yoshiike K, Takemoto KK. Studies with BK virus and monkey lymphotropic papovavirus. In: Salzman NP, ed. The Papovaviridae. New York and London: Plenum Press, 1986:295–326.
Lecatsas G, Schoub BD, Rabson AR et al. Papovavirus in human lymphocyte cultures. Lancet 1976; 2(7991):907–8.
Possati L, Rubini C, Portolani M et al. Receptors for the human papovavirus BK on human lymphocytes. Arch Virol 1983; 75(1–2):131–6.
Seganti L, Mastromarino P, Superti F et al. Receptors for BK virus on human erythrocytes. Acta Virol 1981; 25(4):177–81.
Sinibaldi L, Viti D, Goldoni P et al. Inhibition of BK virus haemagglutination by gangliosides. J Gen Virol 1987; 68(Pt 3):879–83.
Sinibaldi L, Goldoni P, Pietropaolo V et al. Involvement of gangliosides in the interaction between BK virus and Vero cells. Arch Virol 1990; 113(3–4):291–6.
Sinibaldi L, Goldoni P, Pietropaolo V et al. Role of phospholipids in BK virus infection and haemagglutination. Microbiologica 1992; 15(4):337–44.
Johnsen JI, Seternes OM, Johansen T et al. Subpopulations of noncoding control region variants within a cell culturepassaged stock of BK virus: Sequence comparisons and biological characteristics. J Gen Virol 1995; 76(Pt 7):1571–81.
Moens U, Johansen T, Johnsen JI et al. Noncoding control region of naturally occurring BK virus variants: Sequence comparison and functional analysis. Virus Genes 1995; 10(3):261–75.
Chakraborty T, Das GC. Identification of HeLa cell nuclear factors that bind to and activate the early promoter of human polyomavirus BK in vitro. Mol Cell Biol 1989; 9(9):3821–8.
zur Hausen H, Gissmann L. Lymphotropic papovavirus isolated from African green monkey and human cells. Microbio Immunol 1979; 167:137–53.
Takemoto KK, Furuno A, Kato K et al. Biological and biochemical studies of African green monkey lymphotropic papovavirus. J Virol 1982; 42(2):502–9.
Mosthaf Luitgard, Pawlita Michael, Gruss Peter. A viral enhancer element specifically active in human haematopoietic cells. Science 1985; 315:587–600.
Pawlita M, Clad A, Hausen H. Complete DNA sequence of lymphotropic papovavirus: Prototype of a new. Virology 1985; 143:196–211.
Pawlita M, Mosthaf L, Clad A et al. Genome structure and host range restriction of the lymphotropic papovavirus (LPV): Identification of a viral lymphocyte specific enhancer element. Curr Top Microbiol Immunol 1984; 113:26–30.
Pawlita M, Lenoir G, zur Hausen H. Host range restriction of the lymphotropic papova virus (LPV) in cells of human hematopoietic origin. Haematologica 1987; 72(6 Suppl):71.
Haun G, Keppler OT, Bock CT et al. The cell surface receptor is a major determinant restricting the host range of the B-lymphotropic papovavirus. J Virol 1993; 67:7482–92.
Kanda T, Furuno A, Yoshiike K. Mutation in the VP-1 gene is responsible for the extended host range of a monkey B-lymphotropic papovavirus mutant capable of growing in T-lymphoblastoid cells. J Virol 1986; 59(2):531–4.
Kanda T, Takemoto KK. Monkey B-lymphotropic papovavirus mutant capable of replicating in T-lymphoblastoid cells. J Virol 1985; 55(1):96–100.
Herrmann M, Oppenlander M, Pawlita M. Fast and high affinity binding of B-lymphotropic papovavirus to human B-lymphoma cell lines. J Virol 1995; 69:6797–804.
Keppler OT, Herrmann M, Oppenlander M et al. Regulation of susceptibility and cell surface receptor for the B-lymphotropic papovavirus by N glycosylation. J Virol 1994; 68:6933–39.
Erselius JR, Jostes B, Hatzopoulos AK et al. Cell-type-specific control elements of the lymphotropic papovavirus enhancer. J Virol 1990; 64(4):1657–66.
Petterson M, Schaffner W. A purine-rich DNA sequence motif present in SV40 and lymphotropic papovavirus binds a lymphoid-specific factor and contributes to enhancer activity in lymphoid cells. Genes Dev 1987; 1(9):962–72.
Sweet B, Hilleman M. The vacuolating virus, SV40. Proc Soc Exp Biol Med 1960; 105:420.
Barbanti-Brodano G, Trabanelli C, Lazzarin L et al. [SV40 as a possible cofactor in the etiopathogenesis of mesothelioma and other human tumors]. G Ital Med Lav Ergon 1998; 20(4):218–24.
Carbone M, Rizzo P, Procopio A et al. SV40-like sequences in human bone tumors. Oncogene 1996; 13(3):527–35.
Ilyinskii PO, Daniel MD, Horvath CJ et al. Genetic analysis of simian virus 40 from brains and kidneys of macaque monkeys. J Virol 1992; 66(11):6353–60.
Horvath CJ, Simon MA, Bergsagel DJ et al. Simian virus 40-induced disease in rhesus monkeys with simian acquired immunodeficiency syndrome. Am J Pathol 1992; 140(6):1431–40.
Lednicky JA, Arrington AS, Stewart AR et al. Natural isolates of simian virus 40 from immunocompromised monkeys display extensive genetic heterogeneity: New implications for polyomavirus disease. J Virol 1998; 72(5):3980–90.
Shein HM, Enders JF. Multiplication and cytopathogenicity of Simian vacuolating virus 40 in cultures of human tissues. Proc Soc Exp Biol Med 1962; 109:495–500.
O’Neill FJ, Carroll D. Amplification of papovavirus defectives during serial low multiplicity infections. Virology 1981; 112(2):800–3.
O’Neill FJ, Xu XL, Miller TH. Host range determinant in the late region of SV40 and RF virus affecting growth in human cells. Intervirology 1990; 31(2–4):175–87.
Clayson ET, Compans RW. Characterization of simian virus 40 receptor moieties on the surfaces of Vero C1008 cells. J Virol 1989; 63:1095–100.
Atwood WJ, Norkin LC. Class I major histocompatibility proteins as cell surface receptors for simian virus 40. J Virol 1989; 63:4474–77.
Wong GH, Bartlett PF, Clark-Lewis I et al. Inducible expression of H-2 and Ia on brain cells. Nature 1984; 310:688–91.
Breau WC, Atwood WJ, Norkin LC. Class I major histocompatibility proteins are an essential component of the simian virus 40 receptor. J Virol 1992; 66:2037–45.
Basak S, Turner H, Compans RW. Expression of SV40 receptors on apical surfaces of polarized epithelial cells. Virology 1992; 190:393–402.
Laimins LA, Khoury G, Gorman C et al. Host-specific activation of transcription by tandem repeats from simian virus 40 and Moloney murine sarcoma virus. Proc Natl Acad Sci USA 1982; 79(21):6453–7.
Farrell ML, Mertz JE. Cell type-specific replication of simian virus 40 conferred by hormone response elements in the late promoter. J Virol 2002; 76(13):6762–70.
Zullo J, Stiles CD, Garcea RL. Regulation of c-myc and c-fos mRNA levels by polymavirus: Distinct roles for the capsid protein VP1 and the viral early proteins. Proc Natl Acad Sci USA 1987; 84:1210–14.
Dangoria NS, Breau WC, Anderson HA et al. Extracellular simian virus 40 induces an ERK/MAP kinase-independent signalling pathway that activates primary response genes and promotes virus entry. J Gen Virol 1996; 77(Pt 9):2173–82.
Querbes W, Benmerah A, Tosoni D et al. A JC virus induced signal is required for infection of glial cells by a clathrin and eps15 dependent pathway. J Virol 2004; 78(1):250–256.
Chen Y, Norkin LC. Extracellular Simian Virus 40 transmits a signal that promotes virus enclosure within caveolae. Exp Cell Res 1999; 246(1):83–90.
Pelkmans L, Puntener D, Helenius A. Local actin polymerization and dynamin recruitment in SV40-induced internalization of caveolae. Science 2002; 296(5567):535–9.
Spence SL, Pipas JM. Simian virus 40 large T antigen host range domain functions in virion assembly. J Virol 1994; 68(7):4227–40.
Author information
Authors and Affiliations
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2006 Eurekah.com and Springer Science+Business Media
About this chapter
Cite this chapter
Ashok, A., Atwood, W.J. (2006). Virus Receptors and Tropism. In: Ahsan, N. (eds) Polyomaviruses and Human Diseases. Advances in Experimental Medicine and Biology, vol 577. Springer, New York, NY. https://doi.org/10.1007/0-387-32957-9_4
Download citation
DOI: https://doi.org/10.1007/0-387-32957-9_4
Publisher Name: Springer, New York, NY
Print ISBN: 978-0-387-29233-5
Online ISBN: 978-0-387-32957-4
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)